Complexin2 modulates working memory-related neural activity in patients with schizophrenia

European Archives of Psychiatry and Clinical Neuroscience

Volumn 265, Issue 2, 2015, Pages 137-145

  Hass, Johanna ^a   Walton, Esther ^a   Kirsten, Holger ^b   Turner, Jessica ^c   Wolthusen, Rick ^a,e,f   Roessner, Veit ^a   Sponheim, Scott R ^d   Holt, Daphne ^e,f   Gollub, Randy ^e,f   Calhoun, Vince D ^c,g   Ehrlich, Stefan ^a,e,f  

^a Department of Child and Adolescent Psychiatry ^*  (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c MIND RESEARCH NETWORK   (United States)

^d UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f MASSACHUSETTS GENERAL HOSPITAL   (United States)

^g University of New Mexico   (United States)

Author keywords

Complexin2; Frontoparietal circuit; Imaging genetics; Intermediate phenotype; Schizophrenia; Working memory

Indexed keywords

COMPLEXIN 2; REGULATOR PROTEIN; UNCLASSIFIED DRUG; COMPLEXIN II; NERVE PROTEIN; OXYGEN; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC VARIABILITY; GENOTYPE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; INTRAPARIETAL SULCUS; MAJOR CLINICAL STUDY; MATERNAL DEPRIVATION; NERVE CELL NETWORK; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; SINGLE NUCLEOTIDE POLYMORPHISM; WORKING MEMORY; ADULT; BLOOD; BRAIN; BRAIN MAPPING; CLINICAL TRIAL; COMPLICATION; FEMALE; GENETIC ASSOCIATION STUDY; GENETICS; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; MALE; MEMORY DISORDERS; MIDDLE AGED; MULTICENTER STUDY; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; PRINCIPAL COMPONENT ANALYSIS; RECOGNITION; SHORT TERM MEMORY; VASCULARIZATION; YOUNG ADULT;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ADULT; BRAIN; BRAIN MAPPING; FEMALE; FUNCTIONAL LATERALITY; GENETIC ASSOCIATION STUDIES; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY DISORDERS; MEMORY, SHORT-TERM; MIDDLE AGED; NERVE TISSUE PROTEINS; NEUROPSYCHOLOGICAL TESTS; OXYGEN; POLYMORPHISM, SINGLE NUCLEOTIDE; PRINCIPAL COMPONENT ANALYSIS; RECOGNITION (PSYCHOLOGY); SCHIZOPHRENIA; YOUNG ADULT;

EID: 84925495904     PISSN: 09401334     EISSN: 14338491     Source Type: Journal    
DOI: 10.1007/s00406-014-0550-4     Document Type: Article

References (61)

1. Cardno AG, Gottesman II (2000) Twin studies of schizophrenia: from bow-and-arrow concordances to star wars Mx and functional genomics. Am J Med Genet 97:12–17
2. Gottesman II, Shields J (1976) A critical review of recent adoption, twin, and family studies of schizophrenia: behavioral genetics perspectives. Schizophr Bull 2:360–401
3. Morley S (1983) The stress–diathesis model of illness. J Psychosom Res 27:86–87
4. Walker EF, Diforio D (1997) Schizophrenia: a neural diathesis–stress model. Psychol Rev 104:667–685
5. Hankin BL, Abela JRZ (2005) Development of psychopathology: a vulnerability-stress perspective, 1st edn. Sage, London
6. Bayer TA, Falkai P, Maier W (1999) Genetic and non-genetic vulnerability factors in schizophrenia: the basis of the “two hit hypothesis”. J Psychiatr Res 33:543–548
7. Harrison PJ, Weinberger DR (2005) Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 10:40–68; image 5. doi: 10.1038/sj.mp.4001558
8. Yin D-M, Chen Y-J, Sathyamurthy A et al (2012) Synaptic dysfunction in schizophrenia. Adv Exp Med Biol 970:493–516. doi:10.1007/978-3-7091-0932-8_22
9. Reim K, Wegmeyer H, Brandstätter JH et al (2005) Structurally and functionally unique complexins at retinal ribbon synapses. J Cell Biol 169:669–680. doi:10.1083/jcb.200502115
10. Brose N (2008) For better or for worse: complexins regulate SNARE function and vesicle fusion. Traffic 9:1403–1413. doi:10.1111/j.1600-0854.2008.00758.x
11. Takahashi S, Ujihara H, Huang GZ et al (1999) Reduced hippocampal LTP in mice lacking a presynaptic protein: complexin II. Eur J Neurosci 11:2359–2366
12. Strenzke N, Chanda S, Kopp-Scheinpflug C et al (2009) Complexin-I is required for high-fidelity transmission at the endbulb of Held auditory synapse. J Neurosci 29:7991–8004. doi:10.1523/JNEUROSCI.0632-09.2009
13. Basso M, Giraudo S, Corpillo D et al (2004) Proteome analysis of human substantia nigra in Parkinson’s disease. Proteomics 4:3943–3952. doi:10.1002/pmic.200400848
14. DiProspero NA, Chen E-Y, Charles V et al (2004) Early changes in Huntington’s disease patient brains involve alterations in cytoskeletal and synaptic elements. J Neurocytol 33:517–533. doi:10.1007/s11068-004-0514-8
15. Tannenberg RK, Scott HL, Tannenberg AEG, Dodd PR (2006) Selective loss of synaptic proteins in Alzheimer’s disease: evidence for an increased severity with APOE varepsilon4. Neurochem Int 49:631–639. doi:10.1016/j.neuint.2006.05.004
16. Eastwood SL, Harrison PJ (2000) Hippocampal synaptic pathology in schizophrenia, bipolar disorder and major depression: a study of complexin mRNAs. Mol Psychiatry 5:425–432
17. Sawada K, Barr AM, Nakamura M et al (2005) Hippocampal complexin proteins and cognitive dysfunction in schizophrenia. Arch Gen Psychiatry 62:263–272. doi:10.1001/archpsyc.62.3.263
18. Kishi T, Ikeda M, Suzuki T et al (2006) No association of complexin1 and complexin2 genes with schizophrenia in a Japanese population. Schizophr Res 82:185–189. doi:10.1016/j.schres.2005.12.842
19. Lee HJ, Song JY, Kim JW et al (2005) Association study of polymorphisms in synaptic vesicle-associated genes, SYN2 and CPLX2, with schizophrenia. Behav Brain Funct 1:15. doi:10.1186/1744-9081-1-15
20. Eastwood SL, Harrison PJ (2005) Decreased expression of vesicular glutamate transporter 1 and complexin II mRNAs in schizophrenia: further evidence for a synaptic pathology affecting glutamate neurons. Schizophr Res 73:159–172. doi:10.1016/j.schres.2004.05.010
21. Ayhan Y, Sawa A, Ross CA, Pletnikov MV (2009) Animal models of gene–environment interactions in schizophrenia. Behav Brain Res 204:274–281. doi:10.1016/j.bbr.2009.04.010
22. Yamauchi Y, Qin L-H, Nishihara M et al (2005) Vulnerability of synaptic plasticity in the complexin II knockout mouse to maternal deprivation stress. Brain Res 1056:59–67. doi:10.1016/j.brainres.2005.07.015
23. Radyushkin K, El-Kordi A, Boretius S et al (2010) Complexin2 null mutation requires a “second hit” for induction of phenotypic changes relevant to schizophrenia. Genes Brain Behav 9:592–602. doi:10.1111/j.1601-183X.2010.00590.x
24. Begemann M, Grube S, Papiol S et al (2010) Modification of cognitive performance in schizophrenia by complexin 2 gene polymorphisms. Arch Gen Psychiatry 67:879–888. doi:10.1001/archgenpsychiatry.2010.107
25. Ripke S, O’Dushlaine C, Chambert K et al (2013) Genome-wide association analysis identifies 13 new risk loci for schizophrenia. Nat Genet. doi:10.1038/ng.2742
26. Singh S, Kumar A, Agarwal S et al (2014) Genetic insight of schizophrenia: past and future perspectives. Gene 535:97–100. doi:10.1016/j.gene.2013.09.110
27. Burns J, Job D, Bastin ME et al (2003) Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study. BJP 182:439–443. doi:10.1192/bjp.02.396
28. Deserno L, Sterzer P, Wüstenberg T et al (2012) Reduced prefrontal-parietal effective connectivity and working memory deficits in schizophrenia. J Neurosci 32:12–20. doi:10.1523/JNEUROSCI.3405-11.2012
29. Hall M-H, Smoller JW (2010) A new role for endophenotypes in the GWAS era: functional characterization of risk variants. Harv Rev Psychiatry 18:67–74. doi:10.3109/10673220903523532
30. Ehrlich S, Yendiki A, Greve DN et al (2011) Striatal function in relation to negative symptoms in schizophrenia. Psychol Med 1–16. doi:10.1017/S003329171100119X
31. Gollub RL, Shoemaker JM, King MD et al (2013) The MCIC collection: a shared repository of multi-modal, multi-site brain image data from a clinical investigation of schizophrenia. Neuroinformatics. doi:10.1007/s12021-013-9184-3
32. Manoach DS, Press DZ, Thangaraj V et al (1999) Schizophrenic subjects activate dorsolateral prefrontal cortex during a working memory task, as measured by fMRI. Biol Psychiatry 45:1128–1137
33. Roffman JL, Gollub RL, Calhoun VD et al (2008) MTHFR 677C → T genotype disrupts prefrontal function in schizophrenia through an interaction with COMT 158Val → Met. Proc Natl Acad Sci USA 105:17573–17578. doi:10.1073/pnas.0803727105
34. Fischl B, Salat DH, Busa E et al (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355
35. Ehrlich S, Morrow EM, Roffman JL et al (2010) The COMT Val108/158Met polymorphism and medial temporal lobe volumetry in patients with schizophrenia and healthy adults. Neuroimage 53:992–1000. doi:10.1016/j.neuroimage.2009.12.046
36. Yendiki A, Greve DN, Wallace S et al (2010) Multi-site characterization of an fMRI working memory paradigm: reliability of activation indices. Neuroimage 53:119–131. doi:10.1016/j.neuroimage.2010.02.084
37. Smith SM, Jenkinson M, Woolrich MW et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23(Suppl 1):S208–S219
38. Woolrich MW, Ripley BD, Brady M, Smith SM (2001) Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14:1370–1386. doi:10.1006/nimg.2001.0931
39. Mitsis GD, Iannetti GD, Smart TS et al (2008) Regions of interest analysis in pharmacological fMRI: how do the definition criteria influence the inferred result? Neuroimage 40:121–132
40. Anderson CA, Pettersson FH, Clarke GM et al (2010) Data quality control in genetic case-control association studies. Nat Protoc 5:1564–1573. doi:10.1038/nprot.2010.116
41. Purcell S, Neale B, Todd-Brown K et al (2007) PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559–575. doi:10.1086/519795
42. Howie BN, Donnelly P, Marchini J (2009) A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet 5:e1000529. doi:10.1371/journal.pgen.1000529
43. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2:e190. doi:10.1371/journal.pgen.0020190
44. Price AL, Patterson NJ, Plenge RM et al (2006) Principal components analysis corrects for stratification in genome-wide association studies. Nat Genet 38:904–909. doi:10.1038/ng1847
45. Vilain J, Galliot A-M, Durand-Roger J et al (2013) Environmental risk factors for schizophrenia: a review. Encephale 39:19–28. doi:10.1016/j.encep.2011.12.007
46. Callicott JH, Egan MF, Mattay VS et al (2003) Abnormal fMRI response of the dorsolateral prefrontal cortex in cognitively intact siblings of patients with schizophrenia. Am J Psychiatry 160:709–719
47. Potkin SG, Turner JA, Brown GG et al (2009) Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophr Bull 35:19–31. doi:10.1093/schbul/sbn162
48. Fusar-Poli P, Howes OD, Allen P et al (2010) Abnormal frontostriatal interactions in people with prodromal signs of psychosis: a multimodal imaging study. Arch Gen Psychiatry 67:683–691. doi:10.1001/archgenpsychiatry.2010.77
49. He H, Sui J, Yu Q et al (2012) Altered small-world brain networks in schizophrenia patients during working memory performance. PLoS One 7:e38195. doi:10.1371/journal.pone.0038195
50. MacDonald AW 3rd, Thermenos HW, Barch DM, Seidman LJ (2009) Imaging genetic liability to schizophrenia: systematic review of FMRI studies of patients’ nonpsychotic relatives. Schizophr Bull 35:1142–1162
51. Meda SA, Bhattarai M, Morris NA et al (2008) An fMRI study of working memory in first-degree unaffected relatives of schizophrenia patients. Schizophr Res 104:85–95
52. Van Veelen NMJ, Vink M, Ramsey NF, Kahn RS (2010) Left dorsolateral prefrontal cortex dysfunction in medication-naive schizophrenia. Schizophr Res 123:22–29. doi:10.1016/j.schres.2010.07.004
53. Whitfield-Gabrieli S, Thermenos HW, Milanovic S et al (2009) Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proc Natl Acad Sci USA 106:1279–1284
54. Glahn DC, Ragland JD, Abramoff A et al (2005) Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Hum Brain Mapp 25:60–69
55. Stephan KE, Baldeweg T, Friston KJ (2006) Synaptic plasticity and dysconnection in schizophrenia. Biol Psychiatry 59:929–939. doi:10.1016/j.biopsych.2005.10.005
56. Chandler CH, Chari S, Dworkin I (2013) Does your gene need a background check? How genetic background impacts the analysis of mutations, genes, and evolution. Trends Genet 29:358–366. doi:10.1016/j.tig.2013.01.009
57. Hultman CM, Sparén P, Takei N et al (1999) Prenatal and perinatal risk factors for schizophrenia, affective psychosis, and reactive psychosis of early onset: case–control study. BMJ 318:421–426
58. Khandaker GM, Zimbron J, Lewis G, Jones PB (2013) Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies. Psychol Med 43:239–257. doi:10.1017/S0033291712000736
59. Rehn AE, Rees SM (2005) Investigating the neurodevelopmental hypothesis of schizophrenia. Clin Exp Pharmacol Physiol 32:687–696. doi:10.1111/j.1440-1681.2005.04257.x
60. Sawada K, Young CE, Barr AM et al (2002) Altered immunoreactivity of complexin protein in prefrontal cortex in severe mental illness. Mol Psychiatry 7:484–492. doi:10.1038/sj.mp.4000978
61. Woods SW (2003) Chlorpromazine equivalent doses for the newer atypical antipsychotics. J Clin Psychiatry 64:663–667